Abstract

Insects and plants have coexisted for over 350 million years and their interactions have affected ecosystems and agricultural practices worldwide. Variation in herbivorous insects' virulence to circumvent host resistance has been extensively documented. However, despite decades of investigation, the genetic foundations of virulence are currently unknown. The brown planthopper (Nilaparvata lugens) is the most destructive rice (Oryza sativa) pest in the world. The identification of the resistance gene Bph1 and its introduction in commercial rice varieties prompted the emergence of a new virulent brown planthopper biotype that was able to break the resistance conferred by Bph1. In this study, we aimed to construct a high density linkage map for the brown planthopper and identify the loci responsible for its virulence in order to determine their genetic architecture. Based on genotyping data for hundreds of molecular markers in three mapping populations, we constructed the most comprehensive linkage map available for this species, covering 96.6% of its genome. Fifteen chromosomes were anchored with 124 gene-specific markers. Using genome-wide scanning and interval mapping, the Qhp7 locus that governs preference for Bph1 plants was mapped to a 0.1 cM region of chromosome 7. In addition, two major QTLs that govern the rate of insect growth on resistant rice plants were identified on chromosomes 5 (Qgr5) and 14 (Qgr14). This is the first study to successfully locate virulence in the genome of this important agricultural insect by marker-based genetic mapping. Our results show that the virulence which overcomes the resistance conferred by Bph1 is controlled by a few major genes and that the components of virulence originate from independent genetic characters. The isolation of these loci will enable the elucidation of the molecular mechanisms underpinning the rice-brown planthopper interaction and facilitate the development of durable approaches for controlling this most destructive agricultural insect.

Highlights

  • The coevolution of host plants and their enemies is a dynamic process that has spurred adaptation in both natural and agricultural systems [1,2,3,4,5,6]

  • Virulence of brown planthoppers on rice plants Two N. lugens biotypes were sib-mated for use in this work: Biotype 1 that had been reared on the rice variety TN1, and Biotype 2 that had adapted to feed on the resistant Mudgo rice variety (IRRI, 1976)

  • These results demonstrate that both Biotype 1 and Biotype 2 insects are virulent towards the susceptible TN1 rice variety, but only the Biotype 2 insects have adapted to and are virulent towards Mudgo plants that express the Bph1 resistance gene

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Summary

Introduction

The coevolution of host plants and their enemies is a dynamic process that has spurred adaptation in both natural and agricultural systems [1,2,3,4,5,6]. Selective pressure prompts the host plant to evolve some new resistance character that reduces the damage caused by its enemy; in order to avoid extinction, the enemy must evolve new virulence characters to overcome the plant’s defenses or resistance This process has occurred in the interactions of plants with both pathogens and insects, the latter of which have coexisted with plants for over 350 million years [7]. Virulence in brown planthoppers is defined as the ability to tolerate a given resistant rice variety or host plant resistance gene This first virulent N. lugens population that had adapted to the resistance conferred by the Bph gene was termed Biotype 2. Little is known about the genetic architecture of virulence in herbivorous insects or the evolutionary interactions between plants and their insect pests

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